Central respiratory pattern generation in the bullfrog, Rana catesbeiana

Milsom, William K.; Reid, Scott D.; Meier, Janice T.; Kinkead, Richard

doi:10.1016/s1095-6433(99)00113-0

Cited by 32 publications

(11 citation statements)

References 28 publications

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“…The mechanisms underlying this uncoupling are not known and could be due to poorly understood actions of these drugs on turtle neurotransmitter receptors. Episodic breathing in vertebrates is proposed to be produced by several “elements” or neural networks within the brainstem that produce the burst pattern (single breath), respiratory rhythm (intraepisode oscillatory motor output), and breathing pattern (which turns the respiratory rhythm on or off) (Milsom et al ., 1999; Fong et al ., 2009). Our findings support this general model because these variables can be altered independently in isolated turtle brainstems by applying various drugs.…”

Section: Discussionmentioning

confidence: 99%

Regulation of respiratory-related hypoglossal motor output by α1 adrenergic and serotonin 5-HT3 receptor activation in isolated adult turtle brainstems

Bartman

Johnson

2012

Respiratory Physiology & Neurobiology

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The effects of brainstem α1 adrenergic receptor activation on respiratory control in reptiles are poorly understood. Isolated adult turtle brainstems were exposed to phenylephrine (α1 adrenergic agonist) and respiratory motor bursts were recorded on hypoglossal nerves. Phenylephrine acutely increased burst frequency, amplitude (low concentrations only), and regularity of the time interval between the start of respiratory events (single or clustered bursts), and decreased bursts/respiratory event. Burst frequency and timing changes persisted during a 2.0 h washout. Acute increases in burst frequency and amplitude were blocked by prazosin (α1 adrenergic antagonist). Pretreatment with prazosin and tropisetron (5-HT3 antagonist) blocked the increase in respiratory event regularity, but did not alter the decrease in bursts/respiratory event. Intermittent phenylephrine application (4 × 5.0 min separated by 20 min) did not produce long-lasting changes in burst frequency and amplitude, bursts/respiratory event, or respiratory event regularity. Thus, sustained α1 adrenergic receptor activation in turtle brainstems produces acute and long-lasting changes in respiratory burst frequency and pattern.

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Section: Discussionmentioning

confidence: 99%

Regulation of respiratory-related hypoglossal motor output by α1 adrenergic and serotonin 5-HT3 receptor activation in isolated adult turtle brainstems

Bartman

Johnson

2012

Respiratory Physiology & Neurobiology

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“…Although the value of the amphibian model for electrophysiological investigations of respiratory control development is acknowledged (Belzile et al, 2004;Hedrick, 2005;Kinkead, 1997;Milsom et al, 1999;Vasilakos et al, 2005), we are well aware of the limitations inherent to the use of bath application of pharmacological agents onto brainstem preparations . The results obtained from such approach must be interpreted cautiously since the sites of action of the drugs are unknown, and the pharmacological specificities of the agents used have been characterized in mammals and may not apply equally in amphibians.…”

Section: Critique Of Methodsmentioning

confidence: 99%

Noradrenergic modulation of respiratory motor output during tadpole development: role of α-adrenoceptors

Fournier

Kinkead

2006

Journal of Experimental Biology

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Noradrenaline (NA) is an important modulator of respiratory activity. Results from in vitro studies using immature rodents suggest that the effects exerted by NA change during development, but these investigations have been limited to neonatal stages. To address this issue, we used in vitro brainstem preparations of an ectotherm, Rana catesbeiana, at three developmental stages: premetamorphic tadpoles, metamorphic tadpoles and fully mature adult bullfrogs. We first compared the effects of NA bath application (0.02-10· mol·l -1 ) on brainstem preparations from both pre-metamorphic (Taylor-Köllros stages VII-XI) and metamorphic tadpoles (TK stages XVIII-XXIII) and adult frogs. The fictive lung ventilation frequency response to NA application was both dose-and stage-dependent. Although no net change was observed in the pre-metamorphic group, NA application decreased fictive lung burst frequency in preparations from more mature animals. These effects were attenuated by application of ␣ ␣-adrenoceptor antagonists. Conversely, NA application elicited dose-and stage-dependent increases in fictive buccal ventilation frequency. We then assessed the contribution of ␣ ␣-adrenoceptors towards these responses by applying specific agonists (␣ ␣ 1 : phenylephrine; ␣ ␣ 2 : clonidine; concentration range from 10 to 200· mol·l -1 for both). Of the two agonists used, only phenylephrine application consistently mimicked the lung burst frequency response observed during NA application in each stage group. However, both agonists decreased buccal burst frequency, thus suggesting that other (␤ ␤) adrenoceptor types mediate this response. We conclude that modulation of both buccal and lung-related motor outputs change during development. NA modulation affects both types of respiratory activities in a distinct fashion, owing to the different adrenoceptor type involved.

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“…Most studies in non-mammalian amniotes have focused on frogs (Hedrick, 2005;Vasilakos et al 2006;Wilson et al 2006;Gargaglioni and Milsom, 2007;Kinkead, 2009;Klingler and Hedrick, 2013;Ranohavimparany et al 2014). Frogs exhibit tidal buccal ventilation, involving continuous movement of the buccal cavity (Vasilakos et al 2005) and lung ventilation, phase-locked to buccal ventilation and often occurring in episodes Milsom et al 1999). Each lung breath usually consists of two phases.…”

Section: Introductionmentioning

confidence: 99%

Three brainstem areas involved in respiratory rhythm generation in bullfrogs

Baghdadwala

Duchcherer

Paramonov

et al. 2015

The Journal of Physiology

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Key pointsr For most multiphasic motor patterns, rhythm and pattern are produced by the same circuit elements. For respiration, however, these functions have long been assumed to occur separately.r In frogs, the ventilatory motor pattern produced by the isolated brainstem consists of buccal and biphasic lung bursts. Previously, two discrete necessary and sufficient sites for lung and buccal bursts were identified.r Here we identify a third site, the Priming Area, important for and having neuronal activity correlated with the first phase of biphasic lung bursts.r As each site is important for burst generation of a separate phase, we suggest each major phase of ventilation is produced by an anatomically distinct part of an extensive brainstem network.r Embedding of discrete circuit elements producing major phases of respiration within an extensive rhythmogenic brainstem network may be a shared architectural characteristic of vertebrates.Abstract Ventilation in mammals consists of at least three distinct phases: inspiration, post-inspiration and late-expiration. While distinct brainstem rhythm generating and pattern forming networks have long been assumed, recent data suggest the mammalian brainstem contains two coupled neuronal oscillators: one for inspiration and the other for active expiration. However, whether additional burst generating ability is required for generating other phases of ventilation in mammals is controversial. To investigate brainstem circuit architectures capable of producing multiphasic ventilatory rhythms, we utilized the isolated frog brainstem. This preparation produces two types of ventilatory motor patterns, buccal and lung bursts. Lung bursts can be divided into two phases, priming and powerstroke. Previously we identified two putative oscillators, the Buccal and Lung Areas. The Lung Area produces the lung powerstroke and the Buccal Area produces buccal bursts and -we assumed -the priming phase of lung bursts. However, here we identify an additional brainstem region that generates the priming phase. This Priming Area extends rostral and caudal of the Lung Area and is distinct from the Buccal Area. Using AMPA microinjections and reversible synaptic blockade, we demonstrate selective excitation and ablation (respectively) of priming phase activity. We also demonstrate that the Priming Area contains neurons active selectively during the priming phase. Thus, we propose that three distinct neuronal components generate the multiphase respiratory motor pattern produced by the frog brainstem: the buccal, priming and powerstroke burst generators. This raises the possibility that a similar multi-burst generator architecture mediates the three distinct phases of ventilation in mammals.M.I. Baghdadwala and M. Duchcherer contributed equally to this work.

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Central respiratory pattern generation in the bullfrog, Rana catesbeiana

Cited by 32 publications

References 28 publications

Regulation of respiratory-related hypoglossal motor output by α1 adrenergic and serotonin 5-HT3 receptor activation in isolated adult turtle brainstems

Regulation of respiratory-related hypoglossal motor output by α1 adrenergic and serotonin 5-HT3 receptor activation in isolated adult turtle brainstems

Noradrenergic modulation of respiratory motor output during tadpole development: role of α-adrenoceptors

Three brainstem areas involved in respiratory rhythm generation in bullfrogs

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